International Journal of Primatology

, Volume 38, Issue 5, pp 856–871 | Cite as

You are Not Welcome: Social Exchanges between Female Spider Monkeys (Ateles geoffroyi)

  • Juan Carlos Riveros
  • Colleen M. Schaffner
  • Filippo Aureli
Article

Abstract

Group living leads to competition for food between group members. Two types of intragroup food competition may occur: scramble competition, in which all group members use the same resource, such that feeding opportunities are equal for everyone; and contest competition, in which some group members monopolize resources through aggression and dominance. In species in which females disperse from the natal group and immigrate into other groups, immigrant females increase group size and thus possibly food competition. Under these circumstances, other females may use aggression to discourage new females from joining the group. We assessed the distribution of aggression, embraces, and kisses among female spider monkeys (Ateles geoffroyi) in relation to group tenure. We recorded social interactions during 1688 10-min focal animal samples on 11 females in Santa Rosa, Costa Rica. We found that aggression was rare between long-term resident females and aggression rates were not higher during feeding than in other contexts, suggesting there was little contest competition. Long-term residents and less recently immigrant females showed higher aggression rates toward the most recent immigrants than toward other females, especially during the first months after a female immigrated, which coincided with the dry season. We did not find similar patterns for embrace and kiss. These results suggest that other females target aggression toward the most recent immigrants to reduce scramble competition. This finding suggests that group tenure should be included in socioecological models for species with female dispersal.

Keywords

Aggression Female dispersal Fission–fusion Food competition Tenure 

References

  1. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.CrossRefPubMedGoogle Scholar
  2. Amici, F., Aureli, F., & Call, J. (2008). Fission–fusion dynamics, behavioral flexibility, and inhibitory control in primates. Current Biology, 18, 1415–1419.CrossRefPubMedGoogle Scholar
  3. Amici, F., Call, J., & Aureli, F. (2009). Variation in withholding of information in three monkey species. Proceedings of the Royal Society B: Biological Sciences, 276, 3311–3318.Google Scholar
  4. Asensio, N., Korstjens, A. H., Schaffner, C. M., & Aureli, F. (2008). Intragroup aggression, fission–fusion dynamics and feeding competition in spider monkeys. Behaviour, 145, 983–1001.CrossRefGoogle Scholar
  5. Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in spider monkeys: A multiple-level approach. Behavioral Ecology and Sociobiology, 63, 649–659.CrossRefGoogle Scholar
  6. Asensio, N., Schaffner, C., & Aureli, F. (2015). Quality and overlap of individual core areas are related to group tenure in female spider monkeys. American Journal of Primatology, 77, 777–785.CrossRefPubMedGoogle Scholar
  7. Aureli, F., & Schaffner, C. M. (2002). Relationship assessment through emotional mediation. Behaviour, 139, 393–420.CrossRefGoogle Scholar
  8. Aureli, F., & Schaffner, C. M. (2007). Aggression and conflict management at fusion in spider monkeys. Biology Letters, 3, 147–149.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Aureli, F., & Schaffner, C. M. (2008). Spider monkeys: Social structure, social relationships and social interactions. In C. Campbell (Ed.), Spider monkeys: Behavior ecology & evolution of the genus Ateles (pp. 236–265). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  10. Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., et al (2008). Fission–fusion dynamics: New research frameworks. Current Anthropology, 49, 627–654.Google Scholar
  11. Aureli, F., Schaffner, C. M., Asensio, N., & Lusseau, D. (2012). What is a subgroup? How socioecological factors influence interindividual distance. Behavioral Ecology, 23, 1308–1315.CrossRefGoogle Scholar
  12. Barton, R., Byrne, R., & Whiten, A. (1996). Ecology, feeding competition and social structure in baboons. Behavioral Ecology and Sociobiology, 38, 321–329.CrossRefGoogle Scholar
  13. Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software. doi:10.18637/jss.v067.i01.
  14. Chapman, C. A. (1988). Patterns of foraging and range use by three species of neotropical primates. Primates, 29, 177–194.CrossRefGoogle Scholar
  15. Chapman, C. A. (1990a). Ecological constraints on group size in three species of neotropical primates. Folia Primatologica, 55, 1–9.CrossRefGoogle Scholar
  16. Chapman, C. A. (1990b). Association patterns of male and female spider monkeys: The influence of ecology and sex on social organization. Behavioral Ecology and Sociobiology, 26, 409–414.CrossRefGoogle Scholar
  17. Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70.CrossRefGoogle Scholar
  18. Clutton-Brock, T. H., & Janson, C. H. (2012). Primate socioecology at the crossroads: Past, present, and future. Evolutionary Anthropology, 21, 136–150.CrossRefPubMedGoogle Scholar
  19. Croft, D. P., James, R., & Krause, J. (2008). Exploring animal social networks. Princeton: Princeton University Press.CrossRefGoogle Scholar
  20. Emery Thompson, M., Kahlenberg, S. M., Gilby, I. C., & Wrangham, R. W. (2007). Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park. Animal Behaviour, 73, 501–512.CrossRefGoogle Scholar
  21. Furuichi, T., Yamagiwa, J., & Aureli, F. (Eds.) (2015). Dispersing primate females: Life history and social strategies in male-philopatric species. Berlin: Springer.Google Scholar
  22. Hohmann, G., & Fruth, B. (2000). Use and function of genital contacts among female bonobos. Animal Behaviour, 60, 107–120.CrossRefPubMedGoogle Scholar
  23. Isbell, L. A. (1991). Contest and scramble competition: Patterns of female aggression and ranging behavior among primates. Behavioral Ecology, 2, 143–155.CrossRefGoogle Scholar
  24. Janzen, D. H. (1986). Guanacaste national park: Ecological and cultural restoration. San José: La Universidad Estatal a Distancia.Google Scholar
  25. Kahlenberg, S. M., Thompson, M. E., & Wrangham, R. W. (2008a). Female competition over core areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda. International Journal of Primatology, 29, 931–947.CrossRefGoogle Scholar
  26. Kahlenberg, S. M., Thompson, M. E., Muller, M. N., & Wrangham, R. W. (2008b). Immigration costs for female chimpanzees and male protection as an immigrant counterstrategy to intrasexual aggression. Animal Behaviour, 76, 1497–1509.CrossRefGoogle Scholar
  27. Koenig, A., Scarry, C. J., Wheeler, B. C., & Borries, C. (2013). Variation in grouping patterns, mating systems and social structure: What socio-ecological models attempt to explain. Philosophical Transactions of the Royal Society, B: Biological Sciences, 368, 20120348.CrossRefPubMedCentralGoogle Scholar
  28. Kummer, H. (1971). Primate societies: Group techniques of ecological adaptation. Arlington Heights: AHM Publishing.Google Scholar
  29. Miller, J. A., Pusey, A. E., Gilby, I. C., Schroepfer-Walker, K., Markham, A. C., & Murray, C. M. (2014). Competing for space: Female chimpanzees are more aggressive inside than outside their core areas. Animal Behaviour, 87, 147–152.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mitchell, C. L., Boinski, S., & van Schaik, C. P. (1991). Competitive regimes and female bonding in two species of squirrel monkeys (Saimiri oerstedi and S. sciureus). Behavioral Ecology and Sociobiology, 28, 5–60.CrossRefGoogle Scholar
  31. Nicholson, A. J. (1954). An outline of the dynamics of animal populations. Australian Journal of Zoology, 2, 9–65.CrossRefGoogle Scholar
  32. Nishida, T., Kano, T., Goodall, J., McGrew, W. C., & Nakumura, M. (1999). Ethogram and ethnography of Mahale chimpanzees. Anthropological Science, 107, 141–188.CrossRefGoogle Scholar
  33. Palombit, R. A. (2000). Male-female social relationships and infanticide in animals. In C. P. van Schaik & C. H. Janson (Eds.), Male infanticide and its implications (pp. 240–268). Cambridge: Cambridge University Press.Google Scholar
  34. Palombit, R. A., Cheney, D. L., & Seyfarth, R. M. (2001). Female–female competition for male “friends” in wild chacma baboons, Papio cynecephalus ursinus. Animal Behaviour, 61, 1159–1171.CrossRefGoogle Scholar
  35. Potts, K. B., Watts, D. P., & Wrangham, R. W. (2011). Comparative feeding ecology of two chimpanzee communities in Kibale National Park (Uganda). International Journal of Primatology, 32, 669–690.CrossRefGoogle Scholar
  36. Pruetz, J. D., & Isbell, L. A. (2000). Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behavioral Ecology and Sociobiology, 49, 38–47.CrossRefGoogle Scholar
  37. Pusey, A. E., & Schroepfer-Walker, K. (2013). Female competition in chimpanzees. Philosophical Transactions of the Royal Society, B: Biological Sciences. doi:10.1098/rstb.2013.0077.
  38. Pusey, A., Williams, J., & Goodall, J. (1997). The influence of dominance rank on the reproductive success of female chimpanzees. Science. doi:10.1126/science.277.5327.828.
  39. Ramos-Fernandez, G. (2005). Vocal communication in a fission-fusion society: Do spider monkeys stay in touch with close associates? International Journal of Primatology, 26, 1077–1092.CrossRefGoogle Scholar
  40. R Core Team (2015). R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria.Google Scholar
  41. Rebecchini, L., Schaffner, C. M., & Aureli, F. (2011). Risk is a component of social relationships in spider monkeys. Ethology, 117, 691–699.CrossRefGoogle Scholar
  42. Rimbach, R., Link, A., Montes-Rojas, A., Di Fiore, A., Heistermann, M., & Heymann, E. W. (2014). Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment. American Journal of Primatology, 76, 1049–1061.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Robbins, M. M. (2008). Feeding competition and agonistic relationships among Bwindi Gorilla beringei. International Journal of Primatology, 29, 999–1018.CrossRefGoogle Scholar
  44. Robbins, A. M., & Robbins, M. M. (2015). Dispersal patterns of females in the genus Gorilla. In T. Furuichi, J. Yamagiwa, & F. Aureli (Eds.), Dispersing primate females: Life history and social strategies in male-philopatric species (pp. 75–104). Tokyo: Springer.CrossRefGoogle Scholar
  45. Robbins, M. M., Robbins, A. M., Gerald-Steklis, N., & Steklis, H. D. (2005). Long-term dominance relationships in female mountain gorillas: Strength, stability and determinants of rank. Behaviour, 142, 779–809.CrossRefGoogle Scholar
  46. Santorelli, C. J., Schaffner, C. M., Campbell, C. J., Notman, H., Pavelka, M. S., et al (2011). Traditions in spider monkeys are biased towards the social domain. PloS One. doi:10.1371/journal.pone.0016863.
  47. Schaffner, C. M., & Aureli, F. (2005). Embraces and grooming in captive spider monkeys. International Journal of Primatology, 26, 1093–1106.CrossRefGoogle Scholar
  48. Schaffner, C. M., Rebecchini, L., Ramos-Fernandez, G., Vick, L. G., & Aureli, F. (2012). Spider monkeys (Ateles geoffroyi yucatanensis) cope with the negative consequences of hurricanes through changes in diet, activity budget, and fission–fusion dynamics. International Journal of Primatology, 33, 922–936.CrossRefGoogle Scholar
  49. van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 195–218). Boston: Blackwell.Google Scholar
  50. Scott, J., & Lockard, J. S. (1999). Female dominance relationships among captive western lowland gorillas: Comparisons with the wild. Behaviour, 136, 1283–1310.CrossRefGoogle Scholar
  51. Shimooka, Y. (2015). Association networks and life history of female spider monkeys. In T. Furuichi, J. Yamagiwa, & F. Aureli (Eds.), Dispersing primate females: Life history and social strategies in male-philopatric species (pp. 23–43). Tokyo: Springer.CrossRefGoogle Scholar
  52. Shimooka, Y., Campbell, C. J., Di Fiore, A., Felton, A. M., Izawa, K., et al (2008). Demography and group composition of Ateles. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 329–348). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  53. Slater, K., Schaffner, C., & Aureli, F. (2007). Embraces for infant handling in spider monkeys: Evidence for a biological market? Animal Behaviour, 74, 455–461.CrossRefGoogle Scholar
  54. Slater, K., Schaffner, C. M., & Aureli, F. (2009). Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis). American Journal of Primatology, 71, 21–29.CrossRefPubMedGoogle Scholar
  55. Snaith, T. V., & Chapman, C. A. (2007). Primate group size and interpreting socioecological models: Do folivores really play by different rules? Evolutionary Anthropology, 16, 94–106.CrossRefGoogle Scholar
  56. Stahl, D., & Kaumanns, W. (2003). Food competition in captive female sooty mangabeys (Cercocebus torquatus atys). Primates, 44, 203–216.CrossRefPubMedGoogle Scholar
  57. Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41, 291–309.CrossRefGoogle Scholar
  58. Stevenson, P. R., Quiñones, M. J., & Ahumada, J. A. (1998). Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. International Journal of Primatology, 19, 313–324.CrossRefGoogle Scholar
  59. Symington, M. M. (1990). Fission–fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47–61.CrossRefGoogle Scholar
  60. Thierry, B. (2008). Primate socioecology, the lost dream of ecological determinism. Evolutionary Anthropology, 17, 93–96.CrossRefGoogle Scholar
  61. Townsend, S. W., Slocombe, K. E., Emery Thompson, M., & Zuberbuhler, K. (2007). Female-led infanticide in wild chimpanzees. Current Biology. doi:10.1016/j.cub.2007.03.020.
  62. Utami, S. S., Wich, S. A., Sterck, E. H. M., & van Hooff, J. A. R. A. M. (1997). Food competition between wild orangutans in large fig trees. International Journal of Primatology, 18, 909–927.CrossRefGoogle Scholar
  63. Verderane, M. P., Izar, P., Visalberghi, E., & Fragaszy, D. M. (2013). Socioecology of wild bearded capuchin monkeys (Sapajus libidinosus): An analysis of social relationships among female primates that use tools in feeding. Behaviour, 150, 659–689.CrossRefGoogle Scholar
  64. Vick, L. G. (2008). Immaturity in spider monkeys: A risky business. In C. Campbell (Ed.), Spider monkeys: Behavior ecology & evolution of the genus Ateles (pp. 288–328). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  65. Wakefield, M. L. (2008). Grouping patterns and competition among female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. International Journal of Primatology, 29, 907–929.CrossRefGoogle Scholar
  66. Wittig, R. M., & Boesch, C. (2003). Food competition and linear dominance hierarchy among female chimpanzees of the tai National Park. International Journal of Primatology, 24, 847–867.CrossRefGoogle Scholar
  67. Wrangham, R. W. (1979). On the evolution of ape social systems. Social Science Information, 18, 335–368.CrossRefGoogle Scholar
  68. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.CrossRefGoogle Scholar
  69. Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. New York: Springer Science+Business Media.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Instituto de Neuroetología, Universidad VeracruzanaVeracruzMexico
  2. 2.Research Centre in Evolutionary Anthropology and Palaeoecology, Liverpool John Moores UniversityLiverpoolUK

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